DESCRIPTION (Applicant's Abstract) The study of organelle genes is essential to our understanding of eukaryotic cellular and molecular biology. The proper functioning of organelles in eukaryotic cells involves a precise cooperation between nuclear and organellar genetic systems. Defects in this functioning have direct consequences for human health, as is evident from the intense interest in mitochondrially-inherited diseases. The primary goal of this proposal is to address a fundamental problem in the genetic coevolution of the eukaryotic cell: How are organelle genes functionally transferred to the nucleus during evolution, and what are the tempo, pattern, and consequences of these genetic relocations? All of this work is carried out in plants, which for several reasons should be viewed as a model to study functional gene transfer from organelles to nucleus. We propose to: 1) use DNA hybridization arrays to survey 20,000 species of plants in order to elucidate the fine-scale tempo and pattern of loss (and gain) of mitochondrial genes and introns, and to use these findings as the starting point for many of the more in-depth studies outlined below; 2) test, for several mitochondrial genes, the hypothesis that their many separate losses reflect remarkably high rates of functional gene transfer to the nucleus, and in so doing, to learn more about the mechanisms of functional gene transfer; 3) examine a few cases of gene transfer in-depth in order to characterize intermediate stages of transcompartmental duplication, to determine their persistence and the dynamics of mitochondrial vs. nuclear gene loss and silencing, and to investigate whether transcompartmental duplications are ever fixed; 4) identify plants with highly elevated rates of ongoing gene transfer and test the hypothesis that this is caused by highly elevated rates of reverse transcription; 5) determine whether mitochondrial genomes ever reacquire genes lost through transfer to the nucleus, and if so, whether this occurs by direct return from the nucleus of the same organism, or by lateral transfer from an unrelated organism; and. Our secondary goal is to determine the origin and pattern of transmission of an extraordinarily invasive genetic element - a homing group I intron that we showed has invaded mitochondrial coxi genes over 1,000 times through a massive wave of lateral transfers during recent angiosperm evolution.